Interpretive Summary: A plant virus gene required for plant to plant transmission of virus by the wheat curl mite has been identified. The Sidney 81 strain of Wheat streak mosaic virus (WSMV) was efficiently transmitted from wheat to wheat by the wheat curl mite. Replacement of the Sidney 81 HC-Pro gene with the HC-pro gene of another WSMV strain had no effect on wheat curl mite transmission. In contrast, wheat curl mite transmission was abolished when the WSMV HC-Pro gene was replaced with the corresponding gene derived from different virus species. Using a series of chimeric HC-Pro genes in which various portions of the gene were derived from WSMV or a related virus not transmitted by the wheat curl mite revealed that the amino-terminal half of the HC-Pro protein specified wheat curl mite transmission. Collectively, this study represents the first molecular characterization of plant viral-encoded determinants needed for transmission by an eriophyid mite.

Technical Abstract:
Wheat streak mosaic virus (WSMV), type species of the genus Tritimovirus within the family Potyviridae, is transmitted by the wheat curl mite Aceria tosichella. Despite this unusual taxon of vector, WSMV shares a similar genome organization with aphid transmitted species of the genus Potyvirus. Although both tritimoviruses and potyviruses encode a helper component-proteinase (HC-Pro), required for non-persistent aphid transmission of potyviruses, sequence conservation is low (amino acid identity ~16%) and a role for HC-Pro in semi-persistent transmission of WSMV by eriophyid mites has not been investigated. We previously demonstrated that WSMV strain Sidney 81 (WSMV-S81) tolerated replacement of the HC-Pro cistron with the corresponding cistron from diverse species within the family Potyviridae and that these chimeric WSMV genomes retained the ability to systemically infect wheat. Here, we show that wheat curl mite transmission was abolished by replacement of the WSMV HC-Pro with that of an aphid transmitted potyvirus (Turnip mosaic virus), a rymovirus (Agropyron mosaic virus) vectored by a different eriophyid mite, or a more closely related tritimovirus species (Oat necrotic mottle virus, ONMV) with no known vector. In contrast, both WSMV-S81 and WSMV-S81 bearing the HC-Pro cistron derived from the most distantly related WSMV strain (El Batán 3, 86% amino acid sequence identity) were efficiently transmitted from wheat source plants to wheat test plants by the wheat curl mite. Transmission assays conducted with WSMV-S81 bearing various domains of HC-Pro replaced with the corresponding domain from ONMV revealed that determinants of eriophyid mite transmission map to the 5'-proximal half of the HC-Pro cistron. Collectively, these results indicate that despite limited sequence identity and specialization for transmission by very different vector taxa, HC-Pro remains a critical determinant of vector transmission among highly divergent members of the family Potyviridae.